OCORRÊNCIA E FATORES EPIDEMIOLÓGICOS INDIVIDUAIS E DE REBANHO ASSOCIADOS À CLAUDICAÇÃO BOVINA EM REBANHOS LEITEIROS NO
SUL DO BRASIL
Tese submetida ao Programa de Pós-Graduação em Agroecossistemas da Universidade Federal de Santa Catarina para a obtenção do Grau de Doutor em Agroecossistemas. Orientadora: Profa. Dra. Maria José Hötzel.
Coorientadora: Profa. Dra. Marina A. G. von Keyserlingk.
Florianópolis 2018
da UFSC.
Bran Agudelo, José Alfredo
Ocorrência e fatores epidemiológicos individuais e de rebanho associados à claudicação bovina em rebanhos leiteiros no sul do Brasil / José Alfredo Bran ; orientadora, Maria José Hötzel ,
coorientadora, Marina A. G. von Keyserlingk., 2018. 114 p.
Tese (doutorado) - Universidade Federal de Santa Catarina, Centro de Ciências Agrárias, Programa de Pós-Graduação em Agroecossistemas, Florianópolis, 2018. Inclui referências.
1. Agroecossistemas. 2. Dor. 3. Bem-estar
animal. 4. Epidemiologia. 5. Produção leiteira. I. , Maria José Hötzel. II. von Keyserlingk., Marina A. G.. III. Universidade Federal de Santa Catarina. Programa de Pós-Graduação em Agroecossistemas. IV. Título.
possible; if locomotion is impossible, science falls with it. The Logic of Locomotion, in: The Presocratic philosophers, Jonathan Barnes, 1982
Múltiplas pessoas e instituições fizeram contribuições importantes para a realização da presente pesquisa. Não é possível mencionar todas elas aqui, mas o fato de não mencioná-las em nada desmerece as suas importantes contribuições com o processo de investigação. Em seu devido momento já foi feito o reconhecimento. Por simplicidade, mencionarei só algumas pessoas e, principalmente, instituições que apoiaram a realização da pesquisa:
A Fundação de Amparo à Pesquisa e Inovação do Estado de Santa Catarina (FAPESC) contribuiu com a bolsa de doutorado que me foi outorgada.
O programa “Emerging Leaders in the Americas” me outorgou uma bolsa para um estágio curto no Canadá para formação em Epidemiologia no Departamento de Medicina de Populações na Universidade de Guelph. Dito estágio foi realizado sob orientação da Professora Marina vonKeyserlingk (UBC) e o Professor Stephen LeBlanc (Guelph).
A presente pesquisa foi financiada com recursos públicos, pelo Programa Ciência sem Fronteiras (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq, Brazil, projeto No. 400850/2013-3).
O “Animal Welfare Program” (UBC, Canadá) fez grandes contribuições com múltiplos aspectos logísticos, de planejamento e de formação científica para a realização da presente pesquisa.
O Laboratório de Etologia Aplicada (LETA, UFSC) e todos seus integrantes deram suporte e apoio para a realização da pesquisa durante todo o período de estudo.
A equipe de pesquisa, constituída por aproximadamente quinze pessoas de diversas nacionalidades com diferentes qualificações acadêmicas, foi uma grande fonte de ideias, ensinamentos e apoio que foi além dos aspectos técnicos e logísticos.
Os agricultores, técnicos e pessoas envolvidas na produção leiteira nas áreas de estudo fizeram múltiplas contribuições para a realização da pesquisa e análise dos resultados.
Agradezco a la querida y siempre viva memoria, a la eterna sonrisa y el brazo solidario de profesores, estudiantes, trabajadores, amigos, compañeros, a la Tribu y a otras personas vinculadas a la Universidad de Antioquia y al Sindicato de Maestros de Antioquia: a quienes ya no están y a los que aún persisten. Especialmente, debo mi
medio de la guerra que se llevó en sus brazos una buena parte de humanistas, científicos y de personas que soñaron que soñaban. Agradezco por enseñarnos – a toda una generación – sobre humanismo y solidaridad. Y por enseñarnos que el problema científico no es una entidad de esencia puramente gnoseológica.
A presente pesquisa teve como objetivos avaliar a ocorrência e descrever os fatores epidemiológicos associados à apresentação de claudicação em vacas leiteiras, bem como analisar as perspectivas e ações dos agricultores em relação à ocorrência desse problema em bovinos leiteiros. Foram realizados três estudos em Paraná (50 granjas em confinamento visitadas uma vez) e Santa Catarina (44 granjas a pasto visitadas duas vezes). Todas as vacas lactantes no rebanho foram avaliadas para observar o escore de locomoção. Foram coletados dados em nível individual e de rebanho. Foi realizada uma entrevista com os agricultores com rebanhos a pasto. Foram descritos vários fatores epidemiológicos associados a claudicação bovina (baixo escore corporal, dias em leite, paridade). Outros fatores associados em nível do indivíduo só foram constatados em sistema a pasto (raça, lesões no casco) ou confinado (dias em leite, lesões na pele ao redor das articulações). Os rebanhos com predomínio de raça Holandês e os rebanhos que foram forçados a caminhar muito rápido, tiveram a maior incidência de claudicação nas granjas com acesso ao pasto. O uso de colchões como base do cubículo em freestall e instabilidade (escorregadio) do piso na área de alimentação das vacas foram os fatores associados com maior peso nas análises em rebanhos confinados. A través das entrevistas realizadas com agricultores foi observado que muitos agricultores não são treinados para identificar e fazer um adequado manejo preventivo da claudicação, nem contam com assistência veterinária para resolver esse problema. Muitos agricultores pareciam não estar cientes da magnitude da ocorrência de claudicação nas suas propriedades. Existe uma grande oportunidade para diminuir a ocorrência de claudicação nesse tipo de rebanhos. Estrategias de manejo preventivo da claudicação, supervisão continua dos animais e provisão de conforto para as vacas são praticas que podem reduzir o problema em nível dos rebanhos. É recomendável aumentar o grau de conhecimento e habilidades que os agricultores das regiões visitadas têm em relação à etiologia, prevenção e manejo da claudicação.
Palavras-chave: Dor. Bem-estar Animal. Epidemiologia. Produção
INTRODUÇÃO
A claudicação bovina é um sinal clínico caracterizado pela locomoção anormal. Esse problema é comum nos bovinos leiteiros e afeta seriamente sua saúde e bem-estar. As vacas claudicantes podem ter lesões dolorosas nas extremidades ou danos severos nos tecidos, redução no consumo de alimento, perda de peso, diminuição da produção e falhas reprodutivas que podem levar ao descarte prematuro. A alta ocorrência de claudicação afeta a rentabilidade dos rebanhos devido à diminuição da produção e aos custos dos tratamentos.
A claudicação pode ser causada por diferentes doenças, porém as doenças frequentemente associadas com a claudicação afetam principalmente os cascos ou os tecidos adjacentes às extremidades posteriores dos bovinos e são classificadas como desordens de origem infecciosa (dermatite digital, necrobacilose interdigital) e alterações produzidas por perturbações da formação do tecido córneo do casco (doença da linha branca, úlcera de sola).
Do ponto de vista populacional, diversos fatores têm sido associados à alta ocorrência de claudicação em bovinos leiteiros. Esses fatores são classificados como atributos dos indivíduos (idade ou raça, por exemplo) ou fatores em nível do rebanho como o manejo, a alimentação e o uso de protocolos de higiene e prevenção de afecções podais.
OBJETIVOS
A presente pesquisa teve como objetivos avaliar a ocorrência e descrever os fatores epidemiológicos associados à apresentação de claudicação em vacas leiteiras, bem como analisar as perspectivas e ações dos agricultores em relação à ocorrência desse problema em bovinos leiteiros.
MATERIAIS E MÉTODOS
Foram realizados dois estudos epidemiológicos do tipo transversal para avaliar a ocorrência e os fatores epidemiológicos associados à claudicação em bovinos leiteiros no oeste de Santa Catarina (SC) e na região de Castro no Paraná (PR). Adicionalmente, no oeste de
claudicação em bovinos leiteiros. A amostragem das granjas foi realizada por conveniência.
Em Santa Catarina foram selecionadas 44 granjas de produção de leite com acesso a pasto (> 16 horas por dia). As unidades foram visitadas em duas ocasiões em 2015. Nessa região foram levantados dois indicadores de ocorrência: incidência acumulada no período entre cada visita e a prevalência em cada visita. No Paraná foi realizada uma visita em 50 granjas leiteiras em sistemas de Freestall e Compost-barn durante o ano 2016 e foi calculada a prevalência de claudicação nos rebanhos.
Em cada visita foram realizadas avaliações nos animais: escore de locomoção (1-5), registro de lesões superficiais de casco (SC) e lesões nas extremidades (PR), escore de condição corporal (1–5) e raça. Adicionalmente, foram realizadas avaliações no ambiente (salas de ordenha, corredores, áreas de alimentação e repouso dos animais, áreas de pastagem) usando uma lista de checagem e uma entrevista com os produtores para obter informações sobre manejo, produção e saúde dos animais. Os registros básicos de produção, reprodução e sanidade foram coletados nos rebanhos sempre que estiveram disponíveis. Em SC, a entrevista com os agricultores também incluiu um questionário com perguntas sobre os conhecimentos e ações que os agricultores tinham em relação à ocorrência de claudicação em seus rebanhos.
Os dados foram processados e analisados seguindo procedimentos comumente usados em epidemiologia para descrever e sintetizar informações de eventos de saúde de populações: elaboração de diagramas de causalidade, organização dos dados e eliminação de erros, descrição minuciosa de cada variável, análise lógica e matemática de vieses e de variáveis de confundimento e de intervenção, modelagem estatística com análise univariável (cada fator em relação a cada desfecho) e posteriormente multivariável (cada fator significante [P < 0.2] no teste univariável com cada desfecho). A redução dos modelos estatísticos foi realizada manualmente, descartando uma a uma as variáveis que não foram significantes (P < 0.05) e atualizando o modelo a cada vez. As análises estatísticas de inferência realizadas foram, na sua maioria, modelos mistos: regressões logísticas para análises em nível individual e regressões lineares para análises em nível do rebanho.
Em SC o principal desfecho utilizado nos modelos foi a incidência acumulada no período entre cada visita; em nível individual foi verificado se existia associação entre as variáveis explicativas e a
acumulada em cada rebanho. Cada rebanho foi usado como fator aleatório na análise em nível individual para controlar o efeito de medições realizadas em grupos e para informar ao modelo a estrutura hierárquica do dado; o município onde cada granja estava localizada foi usado como fator aleatório em nível de rebanho para controlar o efeito de agrupação espacial das granjas.
A prevalência de claudicação em cada indivíduo e no rebanho foram os desfechos utilizados para cada nível de análise nos modelos estatísticos ajustados para os dados do PR. Nos modelos em nível do indivíduo foram usados os grupos (baias) de animais aninhados dentro de cada granja como fator aleatório para controlar o efeito da pseudorepetição, modelar o efeito de distribuição espacial e da organização hierárquica do dado. Foram ajustados múltiplos modelos em nível individual: um usando a população total avaliada e três diferentes modelos (por categorias de paridade) usando uma subamostra da população com dados de produção de leite, dias em leite e número de partos. Em nível do rebanho foi realizada uma regressão linear simples. Os modelos estatísticos foram construídos usando o software estatístico R e o pacote lme4.
RESULTADOS E DISCUSSÃO
Claudicação em vacas leiteiras em sistemas com acesso a pasto no Oeste de Santa Catarina
Os rebanhos tiveram, em média, 42 vacas em ordenha, variando de 28 a 74. A incidência acumulada de claudicação (1.110 vacas em 41 rebanhos) foi 29.6% e a prevalência (44 rebanhos) foi 31% (1.633 vacas) e 35% (1.836 vacas) na primeira e segunda visita, respectivamente. A ocorrência de claudicação foi relativamente alta nos rebanhos visitados, o que sugere que a claudicação é um problema presente em rebanhos a pasto e que estratégias de prevenção e controle em nível da população deveriam ser implementadas.
Os casos incidentes foram 4 vezes mais comuns em vacas Holandês do que em vacas Jersey e foram mais comuns em vacas com maior número de lactações (1.4 a 13.1 vezes mais em vacas multíparas do que em vacas de primeiro parto). Vacas com escore corporal baixo (2-2.75 e 3) e com lesões superficiais nos cascos apresentaram 1.1 a 4.7 vezes maior incidência de claudicação do que vacas com escore corporal
avançada sugere que medidas de prevenção e controle devem ser aplicadas nesses indivíduos que são mais susceptíveis. O uso de casqueamento, a alimentação adequada das vacas em cada estágio da lactação e o tratamento oportuno são ações que podem ajudar a diminuir o impacto negativo da claudicação nesses rebanhos.
Os rebanhos de raça Holandês apresentaram, em média, 13.5% maior incidência acumulada de claudicação e para cada 1 km/h de aumento na velocidade de condução das vacas por parte dos agricultores a incidência de claudicação aumentou, em média, 5%. A presença de claudicação em animais e rebanhos de raça Holandês sugere que essa raça pode ser mais suscetível a doenças que produzem claudicação quando manejadas em sistemas de pastoreio. Igualmente, fatores de manejo do rebanho podem estar vinculados à alta ocorrência de claudicação nessa raça: o nível de produção e as estratégias de alimentação do rebanho e especialmente das vacas recém paridas, podem ser fatores que intermeiam a relação entre raça e claudicação. A condução do rebanho a alta velocidade pode estar associada a maior probabilidade de lesão nas extremidades dos animais, mas também pode ser um fator que reflita o cuidado no manejo dos animais por parte de cada agricultor.
Claudicação em vacas leiteiras em sistemas com acesso a pasto: perspectivas e ações dos agricultores no Oeste de Santa Catarina
Nos sistemas de produção com acesso a pasto, os agricultores praticaram poucas medidas preventivas e de controle (casqueamento, uso preventivo de pedilúvios, registro de casos e tratamentos) para doenças que causam claudicação. A maioria dos agricultores (43 em 44) reportou ter tratado em algum momento animais que apresentavam claudicação no seu rebanho. Foi mencionado frequentemente o uso de antibióticos, casqueamentos e produtos de aplicação direta no casco (spray, unguentos) para tratar animais claudicantes. A abordagem terapêutica parece estar baseada preferencialmente no tratamento de casos isolados e em menor medida em estratégias de prevenção e controle em nível de população. Muitos dos agricultores visitados tiveram acesso a serviços e orientação veterinária (pública, da indústria de laticínios, ou privada), porém em nenhum caso mencionaram ter participado em processos de formação ou ter assistência técnica específica para controlar e prevenir claudicação em seus rebanhos. De
valores de prevalência de claudicação severa similares aos reportados pelos pesquisadores que avaliaram a locomoção das vacas. Dezessete agricultores reportaram o mesmo número de vacas com claudicação que foi estimada pelo veterinário como claudicação severa (ICC = 0.8). O fato dos agricultores subestimarem a claudicação pode refletir pouca motivação ou interesse no problema, ou mínimo conhecimento dos impactos do problema na saúde e bem-estar dos animais, talvez como reflexo de pouco acesso a treinamento, informação e orientação técnica nessa área. Poucos agricultores mencionaram que a claudicação fosse o primeiro problema de saúde em seus rebanhos, porém, mencionaram frequentemente que era um dos três problemas de saúde animal mais comuns nos seus rebanhos. Além da claudicação, mastite e falha reprodutiva foram mencionados como importantes problemas de saúde nos rebanhos. Esse achado pode refletir a ordem de priorização dos problemas de saúde do rebanho; assim, se múltiplos problemas de saúde acontecem no rebanho, as estratégias de controle podem ser focadas em problemas mais urgentes e prioritários para cada agricultor. Dessa maneira, um problema menos conhecido e pouco enxergado, pode ser negligenciado. Por outro lado, isso pode sugerir a falta de uma estratégia global de prevenção e controle de doenças nos rebanhos, o que acaba impedindo a visualização das relações entre cada problema de saúde e o bem-estar no rebanho (claudicação e falha reprodutiva podem estar relacionadas) e a aplicação de medidas preventivas padrão (higiene, adequada alimentação, tratamento oportuno de casos, por exemplo) que podem ajudar no controle de diferentes problemas.
Claudicação em vacas leiteiras em sistemas confinados no Paraná Foram visitadas 38 granjas usando sistema freestall e 12 que utilizavam compost-barn, totalizando 13.706 vacas. Cada granja teve, em média, 274 vacas em lactação, variando entre 41 a 901. A prevalência média de claudicação nos rebanhos foi 41%. Os fatores associados com alta frequência de claudicação nas vacas foram o baixo escore corporal, a presença de lesões de pele nas extremidades (região do carpo e do tarso) e o estágio da lactação.
Os seguintes fatores estiveram associados à maior prevalência de claudicação (acima da média estimada pelo modelo: 17.32%) nos rebanhos: a presença de pisos escorregadios nas áreas de alimentação das vacas (6.6% a 12.4%), o uso de colchões nas camas das vacas em
(6.8% a mais em rebanhos com período < 60 dias). Realizar alimentação adequada das vacas para evitar o baixo escore corporal, controlar os fatores que geram lesões superficiais nas extremidades (material da cama, tamanho dos cubículos e limpeza das camas), e a aplicação de medidas preventivas para claudicação, especialmente em novilhas e vacas primíparas, são importantes medidas para reduzir o impacto negativo da claudicação nas vacas. O uso de camas confortáveis nos cubículos e o desenho adequado dos pisos são aspectos relacionadas à estrutura da granja que podem reduzir a prevalência de claudicação nos rebanhos visitados. O tamanho de rebanho é um fator que pode refletir a intervenção de outros fatores na prevalência de claudicação; consequentemente, não deve existir relação causal nessa associação. As diferenças na prevalência de claudicação em vacas com diferentes períodos de secagem podem ser reflexo do manejo das vacas secas, bem como o nível de produção de cada granja; assim, ambos fatores podem ter grande impacto na prevalência de claudicação nos rebanhos.
CONCLUSÕES
A claudicação parece ser um problema comum nos rebanhos e regiões estudadas. A grande variação da ocorrência de claudicação observada entre granjas, municípios e regiões evidencia que práticas de manejo realizadas pelos agricultores em cada lugar podem influenciar a ocorrência do problema e que há uma grande oportunidade para prevenir, controlar e diminuir os impactos negativos desse problema na saúde e bem-estar dos animais e na rentabilidade dos estabelecimentos leiteiros.
Palavras-chave: Dor. Bem-estar animal. Epidemiologia. Produção
Lameness is a clinical sign characterized by locomotion disturbance in dairy cows. Lameness affects the health and welfare of dairy cattle. The aim of this study was to assess the occurrence and associated risk factors to lameness in smallholders grazing dairy herds and in freestall and compost-bedded barns. Additionally, we explore the farmers’ perspectives and actions regarding lameness in their (grazing) herds. The three studies had an epidemiological approach. The studies were conducted in two different geographical regions: forty four grazing dairy farms located in the south of Brazil were visited twice in 2015 and 50 freestall and compost-bedded pack farms were visited once in 2016. All lactating cows present at the moment of the visits were gait scored by a single researcher. Individual-level attributes (e.g., body condition score, milk yield, days in milk, superficial hoof lesions) were collected. A face to face interview was conducted with farmers at the time of the visits. We found some associations between cow- and herd-level variables and lameness that were similar between different dairy systems (confined and grazing), i.e., low body condition score, parity. Other cow-level variables such as breed, and some leg and hoof abnormalities were detected in specific systems, in part due to the sample characteristics. Due to the greater sample size that we explored in the confined dairies we modeled different patterns of lameness distribution in cows across days in milk and parity. We also identified herd-level variables associated with lameness that were different by each housing system. Holstein herds and herds where cows were forced to move to the milking parlor at excessive speeds were associated with the highest incidence of clinical lameness in grazing herds. The use of mattress on freestall cubicles as stall base and the presence of slippery surfaces at the cow-feed alley were the predictors with stronger association with lameness in confined herds. Through the survey conducted with the farmers we found that most of them had no training on lameness management, and cited an overall lack of veterinary support to control lameness on their farms. The farmers seemed unaware of the extent of lameness on their farms. Interventions aimed at reducing lameness in large confined and small scale herds in this region of Brazil should include a preventative veterinary assistance approach focused, in controlling lameness in high risk individuals, promoting cow comfort and the use of animal welfare protocols focused in improving supervision of cow health by the farmers and suitable actions to control
of herds.
Figure 1. Distribution of veterinarian (clinical = locomotion score ≥ 3; severe = locomotion score ≥ 4) and farmer estimated lameness prevalence in 44 small-scale grazing dairy farms located in the south of Brazil visited twice in 2015. Farmer estimated prevalence in the second visit was obtained from 43 farms...62
Table 1. Predictors and outcomes used in the multivariable models for cow- and herd-level analyses of risk factors for lameness in lactating cows assessed twice 4 months apart on 44 small-scale grazing dairy farms located in the south of Brazil...48 Table 2. Description of small-scale grazing dairy farms (n = 44) located in the south of Brazil that were visited twice...49 Table 3. Cow-level risk factors for accumulated incident cases of lameness (locomotion score ≥ 3) in lactating cows (n = 498) observed twice 4 months apart on small-scale grazing dairy farms (n = 40) located in the south of Brazil...50 Table 4. Cow-level risk factors for chronic cases of lameness (locomotion score ≥ 3) in lactating cows (n = 468) observed twice 4 months apart on small-scale grazing dairy farms (n = 40) located in the south of Brazil...51 Table 5. Cow-level risk factors for recovered cases of lameness (locomotion score ≥ 3) in lactating cows (n = 174) observed twice 4 months apart on small-scale grazing dairy farms (n = 37) located in the south of Brazil...52 Table 6. Herd-level risk factors for cumulative incidence of lameness (locomotion score ≥ 3) in 35 small-scale grazing dairy farms visited twice 4 months apart in the south of Brazil...52 Table 7. Questionnaire conducted with farmers in 44 small scale grazing dairy farms located in the south of Brazil...59 Table 8. Associations between severe lameness prevalence estimates provided by a trained veterinarian and those provided by farmers when asked the percentage of lame cows on their farms. Farms (n = 44) were small scale grazing dairies visited twice in 2015 in the south of Brazil.61 Table 9. Farmers’ suggested causes of lameness in 44 small scale grazing dairy farms located in the south of Brazil and visited in 2015.. 63 Table 10. Distribution of estimated clinical lameness (locomotion score ≥3) prevalence by gate scoring by a trained veterinarian between answers of farmers to questions about lameness relevance in the farm in 44 small scale grazing dairy farms visited twice in the south of Brazil in 2015...64 Table 11. Associations between farmers’ answers to questions on farm lameness relevance and prevalence (locomotion score ≥3) by gate scoring by a trained veterinarian on the first and second visit, in 44 small scale grazing dairy farms in the south of Brazil in 2015...65
Table 13. Main features and management practices of 50 confined dairy farms located in Paraná state – south of Brazil that were visited once in 2016...74 Table 14. Distribution of lameness prevalence in herds, pens within herds and by lactating herd size in compost-bedded pack and freestall dairy barns visited once in 2016 and located in the south of Brazil...78 Table 15. Distribution of lameness cases by categories of predictors considered in multivariable models for assessment of cow-level factors associated with lameness prevalence in lactating dairy cows housed in compost-bedded pack (n = 12 herds) and freestall barns (n = 38 herds) visited once in 2016 and located in the south of Brazil...79 Table 16. Distribution of lameness cases by categories of predictors considered in multivariable models for assessment of cow-level factors associated with lameness prevalence in lactating cows housed in compost-bedded pack (n = 39 cows in 1 herd) and freestall barns (n = 5490 cows in 15 herds) visited once in 2016 and located in the south of Brazil...80 Table 17. Distribution of lameness cases by parity and days in milk in lactating dairy cows housed in compost-bedded pack (n = 39 cows in 1 herd) and freestall barns (n = 5490 cows in 15 herds) located in the south of Brazil...81 Table 18. Distribution of lameness prevalence (locomotion score ≥ 3) by categories of predictors considered in multivariable models for assessment of herd-level factors associated with lameness in lactating cows housed in compost-bedded pack (n = 12 herds) and freestall barns (n = 38 herds) visited once in 2016 and located in the south of Brazil.. 83 Table 19. Cow-level factors associated with lameness prevalence (locomotion score ≥ 3) in lactating dairy cows (n = 13706 cows in 50 herds) housed in freestall (n = 12454 cows in 38 herds) and compost-bedded pack barns (n = 1252 in 12 herds) visited once in 2016 and located in the south of Brazil...85 Table 20. Cow-level factors associated with lameness prevalence (locomotion score ≥ 3) in primiparous lactating dairy cows (n = 2002 cows in 16 herds) housed in freestall (n = 15 herds) and compost-bedded pack barns (n = 1 herd) visited once in 2016 and located in the south of Brazil...86 Table 21. Cow-level factors associated with lameness prevalence (locomotion score ≥ 3) in second-lactation dairy cows (n = 1438 cows in
Brazil...87 Table 22. Cow-level factors associated with lameness prevalence (locomotion score ≥ 3) in multiparous (> second parity) dairy cows (n = 1920 cows in 16 herds) housed in freestall (n = 15 herds) and compost-bedded pack barns (n = 1 herd) visited once in 2016 and located in the south of Brazil...88 Table 23. Herd-level factors associated with lameness prevalence (locomotion score ≥ 3) in lactating dairy cows housed in freestall (n = 37 herds) and compost-bedded pack barns (n = 10 herds) visited once in 2016 and located in the south of Brazil...89
1 INTRODUCTION 29
1.1 STUDY OBJECTIVES...30
2 LAMENESS IN DAIRY COWS: A BRIEF REVIEW 31 2.1 LAMENESS IMPACTS IN DAIRY HERDS...33
2.2 LAMENESS CLASSIFICATIONS AND RISK FACTORS...34
2.3 COW COMFORT ISSUES: LYING, STANDING, AND FACILITIE’S DESIGN AND CONDITION...35
2.4 EFFECTS OF NUTRITIONAL MANAGEMENT, MILK YIELD, BODY CONDITION SCORE AND PHYSIOLOGICAL STATUS OF THE TRANSITION COW ON LAMENESS...36
2.5 GRAZING, OUTDOOR ACCESS AND LAMENESS...39
3 COW- AND HERD-LEVEL FACTORS ASSOCIATED WITH LAMENESS IN SMALL-SCALE GRAZING DAIRY HERDS IN BRAZIL 43 3.1 INTRODUCTION...43
3.2 MATERIALS AND METHODS...43
3.2.1 Animal-based evaluations...44
3.2.2 Management and environment based evaluations...45
3.2.3 Data Analyses...45
3.3 RESULTS...47
3.3.1 Descriptive statistics...47
3.3.2 Cow-level factors associated with lameness...50
3.3.3 Herd-level factors associated with lameness...51
3.4 DISCUSSION...52
3.5 CONCLUSION...56
4 LAMENESS ON BRAZILIAN PASTURE BASED DAIRIES: FARMERS’ AWARENESS AND ACTIONS 57 4.1 INTRODUCTION...57
4.2 MATERIALS AND METHODS...57
4.2.4 Data analyses...60
4.3 RESULTS...60
4.3.1 Characterization of the families...60 4.3.2 Farmers’ estimated lameness prevalence...61 4.3.3 Farmers’ suggested causes of lameness in dairy cows...62 4.3.4 Farmers’ sources of information...63 4.3.5 Lameness as a health issue or a reason for culling cows...63 4.3.6 Veterinary assistance, prevention measures and treatments applied for lameness in the farms...64
4.4 DISCUSSION...66 4.5 CONCLUSION...70
5 ASSOCIATIONS BETWEEN COW- AND HERD-LEVEL RISK FACTORS AND LAMENESS PREVALENCE IN FREESTALL AND COMPOST-BEDDED PACK DAIRY BARNS
IN SOUTHERN BRAZIL 71
5.1 INTRODUCTION...71 5.2 MATERIALS AND METHODS...71
5.2.1 Animal-based evaluations...72 5.2.2 Interview on herd management...72 5.2.3 Farm inspection...73 5.2.4 Data analyses...73
5.3 RESULTS...77
5.3.1 Data description...77 5.3.2 Cow-level factors associated with lameness...77 5.3.3 Herd-level factors associated with lameness...89
5.4 DISCUSSION...90 5.5 CONCLUSION...96
6 GENERAL CONCLUSIONS 97
OVERVIEW
The present manuscript is composed by three chapters with data derived from two observational sectional studies and one cross-sectional survey. The studies were conducted in two different regions located in the south of Brazil (Paraná and Santa Catarina States). Both regions are important in terms of dairy industry development in Brazil. For our knowledge, this is the first great epidemiological study on lameness in dairy cows conducted in Brazil.
The fist chapter describes the results of a cross-sectional study designed to assess the occurrence and the associations with lameness in cows in small-scale grazing dairy herds. This chapter was published as a research paper on the Journal Preventive Veterinary Medicine (BRAN et al., 2018b). The data and R-code that was used to run the main analyses of the study have also been published (BRAN et al., 2018d).
The second chapter describes the results of cross-sectional survey that was designed to investigate the farmers’ perspectives and actions regarding lameness occurrence, prevention and control at the same farms where the lameness occurrence was assessed (i.e., first study). This chapter has been published in the Journal Preventive Veterinary Medicine (BRAN et al., 2018a). The data and R-code that was used to run the main analyses of the study have been published (BRAN et al., 2018c).
The third chapter describes the results of a cross-sectional study designed to assess the occurrence and the associations with lameness in dairy cows and herds in small, medium and large dairies using freestall and compost-bedded barns, located in Paraná State. This chapter is in publication process.
During the study process, the research team also focused efforts in working together with farmers and dairy industry stakeholders (public and private). We were able to socialize the research with people involved in dairy industry at the regions and mainly with the farmers. Didactic material and several meetings were conducted at the regions in order to be coherent with the scientific principle of humanism and social retribution of science to the communities. On-line information for extension purposes was disclosed and a permanent link is active: http://cartilhaonline.wixsite.com/letaufsc/bemestaranimal.
This thesis was part of a larger project funded by the Brazilian government through the Program Science Without Borders (Grant
MEC/MCTI/CAPES/CNPq/FAPsnº71/2013, Animal welfare: A necessary component for sustainability of Brazilian dairy industry).
1 INTRODUCTION
Lameness is a common issue that impairs health and welfare of dairy cattle. Cows affected by lameness have low dry matter intake and milk yield (BACH et al., 2007; BICALHO; WARNICK; GUARD, 2008), low risk of pregnancy (ALAWNEH; LAVEN; STEVENSON, 2011) and high risk of being culled (BICALHO et al., 2007). Economic losses in the affected herds are associated with treatment costs and specially to reduction of productivity (BRUIJNIS; HOGEVEEN; STASSEN, 2013; HUXLEY, 2013).
Lameness is a clinical sign characterized by locomotion disturbance in dairy cows (O ’CALLAGHAN, 2002) . Gait pattern modification in lame cows results from a compensatory posture, or adjusts in weight distribution during gait, in response to inadequate corporal balance, lesions, or pain associated mainly with orthopedic origin (hooves, joints, muscles). Thus, visual indicators are commonly used in order to assess if an individual is affected: the symmetry of limb's movement, gait's rhythm and speed, weight bearing on extremities, or abnormal postures (FLOWER; WEARY, 2009).
Most cases of lameness originate in lesions of the lateral claws on the hind feet (BLOWEY; WEAVER, 2011; POTTERTON et al., 2012). This pattern might be explained partly by the overloading of the softer parts of the lateral hind claws on normal gait (VAN DER TOL et al., 2002), by the asymmetric nature of bovine toes (lateral toes are longer than medial and, on hard surfaces, receive more weight) (MUGGLI et al., 2011) and by the changing padding capacity of digital cushion in different ages and days of lactation (lower padding in old cows and around lactation peak) (RÄBER et al., 2004; LIM et al., 2015).
Lameness may be the consequence of multiple diseases and some infectious agents have been identified as causes of lameness (REFAAI et al., 2013), but also non infectious causes of lameness have been described. The action of traumatic forces might affect selectively the limbs of individuals in higher risk (i.e., old cows on weeks around calving) and result in foot lameness (GREEN et al., 2014; LIM et al., 2015; RANDALL et al., 2015). The etiology of lameness is multifactorial and complex, but, in general, the interaction of two main factors appears to strongly influence the dynamics of non infectious lameness related to claw horn disruption: cow comfort issues, mainly related to environmental variables (i.e., inadequate size of facilities, overstocking, inappropriate floor, paths and lying surfaces
characteristics) (BUROW et al., 2014; SOLANO et al., 2015, 2016; RANJBAR et al., 2016; WESTIN et al., 2016a) and the relationship between physiological changes during transition period and nutritional management of the herd (i.e., fast loss of body weight and deficient feeding of cows around calving) (DIPPEL et al., 2009; BICALHO; OIKONOMOU, 2013; ALAWNEH et al., 2014).
Access to pasture or loafing areas has been reported as protective factors for lameness in confined dairy cows (HERNANDEZ-MENDO et al., 2007; OLMOS et al., 2009a; GARD et al., 2015). However, studies assessing lameness in grazing dairy herds, are scarce. Possible protective effect of grazing for lameness, might be due to reduction of risk for specific lesions or diseases (i.e., sole ulcer), but, in turn, some factors in grazing systems may potentially increase the probability of lameness occurrence.
Condition of paths, heat stress, or other comfort-related issues could be trigger factors increasing the occurrence of lameness by enhancing risk factors for diseases like white line disease, foot root or digital dermatitis. In fact, hoof lesions such as white line disease, sole injury and axial disease, seems to be more common in grazing cows (LAWRENCE; CHESTERTON; LAVEN, 2011) and sole damage (i.e., sole ulcer, double sole) has been found commonly in housed systems, if compared with grazing systems (NAVARRO; GREEN; TADICH, 2013). Also, access to pasture in cows housed in tie stall was associated with higher presence of digital dermatitis, white line separation and interdigital fibroma (CRAMER et al., 2009). Hence the risk factors for lameness, or the relative importance of specific exposures might differ between housing systems.
1.1 STUDY OBJECTIVES
The present study aimed to a) investigate the occurrence of lameness in dairy herds in southern Brazil and b) to describe the associated risk factors both at the cow- and herd-level. Additionally, c) we explored the way that farmers deal with lameness (i.e., prevention and control) in dairy cows and how aware they were regarding lameness occurrence and impacts at their farms.
2 LAMENESS IN DAIRY COWS: A BRIEF REVIEW
Lameness in cattle is the manifestation of abnormal locomotion, that is often associated with tissue damage, pain and discomfort (O’CALLAGHAN, 2002). However, lameness is not always an issue restricted to pain and evident tissue damage. Although most cases of lameness might be associated with pain or tissue damage, in some instances there is no evidence of macroscopic lesions and pain is not always demonstrable in lame cows; also, claw lesions are present in non-lame cows (DYER et al., 2007; TADICH; FLOR; GREEN, 2010).
In the cases where pain or macroscopic tissue damage cannot be demonstrated, lameness is still a problem: postural or gait dysfunctions might be a primary problem which affects all the perceptual-behavioral repertory (dry matter intake, resting, socialization) of the animal and may lead to secondary problems derived from muscular or articular overuse and underuse in different body parts (the back, contralateral or ipsilateral structures to affected limb may be affected). Also, uneasy venous return on extremities, pain on different structures than affected limb (i.e., back pain), chronic degeneration of structures, atrophy and compensatory hypertrophy of muscles and articular structures might be dysfunctions resulting from postural abnormalities.
Pain is an important issue associated with lameness, but some physiopathological alterations of nociceptive threshold, the subjectivity associated with pain experience, the neural plasticity, or the multiple forms of pain (MILLMAN, 2013) (i.e., acute or chronic, nociceptive or inflammatory, pathological or physiological) might be also taken in consideration when assessing the relationship between lameness and pain. Allodynia and hyperalgesia, for example, might be present in a limping cow (O’CALLAGHAN, 2002; NAVARRO; GREEN; TADICH, 2013; SHEARER, 2017) and the health and welfare consequences for individuals with those problems are also as important as the responses of individuals with unaltered nociception (PRESCOTT; MA; DE KONINCK, 2014).
In addition, information about automatic or objective pain quantification in lame dairy cattle is still scarce and most of the information about lameness is derived from visual locomotion assessment. This is a main issue when assessing and interpreting the results of lameness studies derived from visual assessment since inferences about nociception are hardly extracted without using deep clinical exploration of the lame individual (DYER et al., 2007;
BLACKIE et al., 2013). In addition locomotion scores are subjective and different scores are adopted by researchers which may limit the comparisons between studies conducted in diverse conditions and contexts.
The ongoing challenges associated with high rates of lameness in cows are of great concern for the global dairy industry. This malady negatively impacts animal health, animal welfare, milk production and the herds’ economic performance (GREEN, 2012; GREEN et al., 2014). Considering the magnitude of this problem, and the fact that lame cows are in pain (COETZEE et al., 2017) this phenomenon constitute a serious animal welfare problem at the population level. Lameness is often used as a main indicator of dairy cow welfare status on farms in many assurance programs, since it is a multicausal issue (GREEN, 2012). Thus, any intervention that can control this problem should impact the overall status of a dairy cows’ health and welfare.
The main causes of lameness in dairy cows are claw horn disruption diseases (e.g., sole ulcer or white line separation) and infectious diseases affecting the foot (e.g., digital dermatitis, interdigital necrobacillosis) (HUXLEY et al., 2012). Claw horn disruption diseases are affected by the physiological effects happening around calving, for instance, increased laxity of the hoof suspensory apparatus (TARLTON et al., 2002), lactogenesis and decreases in body condition score (BCS), and reduced thickness of sole soft tissues (digital cushion and corium) (NEWSOME et al., 2017a, 2017b).
Additionally, biomechanical issues affecting the horn and the suspensory apparatus of the third phalanx, or any factor that potentially increases friction by excessive hoof wear and by abnormal weight distribution can predispose cows to claw injuries. Claw lesions are strongly associated with contusions within the horn (BICALHO; MACHADO; CAIXETA, 2009) that may affect the germinal epithelium that produces the horn, causing a disruption in the normal horn formation. The lateral hind claws are commonly affected by lesions, given that these structures normally support greater pressure (VAN DER TOL et al., 2002).
The causal pathways linking the specific conditions with the occurrence of lameness are mediated by diverse environmental factors and specific characteristics of the individual cows, which are continuously changing over time and thus may be linked to greater susceptibility periods, or places with greater exposures to the risk factors. Some farm characteristics such as management practices and
individual features associated with the occurrence of lameness in dairy cows have been described in different populations (CHAPINAL et al., 2014; SOLANO et al., 2015; NEWSOME et al., 2017a). Overall, any environmental factor that may cause, or increase the risk of hoof infection (e.g., presence of the infectious agent, exposure of cows to dirt and wet floors), or causes excessive stress and overloading of hooves in the cows (e.g., exposure to hard lying or walking surfaces, hoof overgrowth) may potentially increase the occurrence of lameness. 2.1 LAMENESS IMPACTS IN DAIRY HERDS
Some of the secondary problems associated with lameness in dairy cows are: a) reduction of dry matter intake and milk yield (BACH et al., 2007; BICALHO; WARNICK; GUARD, 2008); b) decrease of the risk of pregnancy (BICALHO et al., 2007; ALAWNEH; LAVEN; STEVENSON, 2011); c) cows affected by lameness also have high risk of being culled prematurely (BICALHO et al., 2007) due to lower production, or due to animal welfare considerations; d) also, there is considerable increase in the cost of treatments of lame cows (BRUIJNIS; HOGEVEEN; STASSEN, 2013) in farms affected by lameness.
Lame cows reduce both feed intake and the time they spent feeding (NORRING et al., 2014). Milk losses due to lameness were estimated to be between 314 and 424 kg/cow per 305 days lactation (BICALHO; WARNICK; GUARD, 2008). Severe lame cows have their potential (305 days in milk) yield reduced by 350 kg or 650 kg if they are observed lame in the first or the first two consecutive months of lactation, respectively (ARCHER; GREEN; HUXLEY, 2010). In addition, it has been reported reductions of milk yield between 0.5 to 1.5 kg/day after lameness diagnosis (WARNICK et al., 2001). However, the decrease in milk yield is not easily observed immediately before or after the lameness event, which might mask the effect of lameness on production when assessed by the farmers or their advisers. The greatest impact of lameness in production is associated with milk yield reduction in the whole lactation (ARCHER; GREEN; HUXLEY, 2010) which requires an in deep exploration of herd performance. Treating lame cows, however, is associated with increases in milk yield (ARCHER; GREEN; HUXLEY, 2010).
The daily risk of conception for lame grazing cows decreased by a factor of 0.78, which means that lame cows take more 12 days for
became pregnant than unaffected cows (ALAWNEH; LAVEN; STEVENSON, 2011). Additionally, lame cows are at a 15% lower risk of pregnancy than nonlame cows (BICALHO et al., 2007).
Some aspects of housing system, or different herd level characteristics (“herd management”) are important modulators of lameness occurrence. Some individual features of dairy cows such as age, milk yield, body conformation, or the rate of body condition score loss, may be important risk factors for lameness. The dynamic interaction between different factors on those complementary levels of analysis (population and individual) determines the occurrence of lameness in dairy herds. Hence, both levels should be considered in order to better understand the dynamics of lameness in dairy herds. 2.2 LAMENESS CLASSIFICATIONS AND RISK FACTORS
There are different classifications of lameness in dairy cows, however, those categories are not necessarily exclusive or rigid. Given the multi causal, progressive and dynamic characteristics of some conditions that cause lameness, most definitions can be complementary, or may express the dynamics of progression of a specific disease; i.e, lameness in the foot may affect muscles, joints and nerves and so, a lameness case that was originated in the hoof might compromise extra-hoof structures.
Most lameness events have a relationship with hoof disorders, thus, it is usual to classify lameness by an anatomical criteria as foot lameness and upper limb lameness (BLOWEY; WEAVER, 2011). Other common classification of lameness is based on their etiology, as infectious and non-infectious: most of those being associated with hoof lesions (HUXLEY et al., 2012; REFAAI et al., 2013). Infectious agents might grow on the hoof, or on the skin around it, and result in foot lameness. Environmental conditions such as high soil moisture and lack of hygiene on stalls or floors might be important reservoirs of pathogens that infects the hoof. On the other hand, non infectious agents like traumatic forces interact with metabolic and physiological status of the cows to induce foot lameness associated with claw horn disruption lesions (CHDL). Two main factors appear to strongly influence the occurrence of non infectious lameness: cow comfort issues, mainly related to environmental variables (SOLANO et al., 2016; WESTIN et al., 2016a) and the relationship between physiological changes that
occur during the transition period (four weeks around the parturition) and the nutritional management of the herd (DIPPEL et al., 2009). 2.3 COW COMFORT ISSUES: LYING, STANDING, AND FACILITIE’S DESIGN AND CONDITION
Excessive or prolonged stress induced by forces acting on the hooves or other body structures responsible for cows’ movement (muscles, joints, nerves), might impact the normal locomotion of dairy cows. Lying behavior alterations are associated with lameness in dairy cows in two opposite ways: like a possible cause and as a consequence. Evidence for the last effect is strongly because information from cross-sectional studies on lameness is found frequently, but analysis of lying behavior preceding the event of lameness is lacking. However is accepted that any affecting normal lying time or lying comfort (i.e., high temperature, uncomfortable surfaces for lying, overstocking) might enhance the stress over the hooves and, eventually, may result in CHDL and lameness.
Decreasing lying comfort and observation of abnormal lying postures are also associated with increases in lameness occurrence (DIPPEL et al., 2009). Lame cows have longer lying times and fewer and longer lying bouts than nonlame cows (ITO et al., 2010; SEPÚLVEDA-VARAS; WEARY; VON KEYSERLINGK, 2014; WESTIN et al., 2016a). Also herds with higher lameness prevalence have longer mean daily lying time (SOLANO et al., 2016). The prolonged lying time in lame cows might be a response to discomfort and pain associated with lameness and may be responsible for most part of the reduction in feeding and weight lost in lame cows.
Allowing the cows to access comfortable facilities seems to increase lying times in cows with limitations for lying, and this can be a protective factor for lameness, possibly by reducing the trauma or concussion of the hoof and by avoiding venous stasis or higher hydrostatic pressure on the feet of the cow. Offering more space on stall (≥114 cm wide), feed alleys ( ≥350 cm wide), as well as using sand (WESTIN et al., 2016a) or higher depth of bedding materials on stalls is associated with increases in the cows’ lying time (SOLANO et al., 2016). The use of mattress on stalls is associated with higher lameness occurrence (ITO et al., 2010). Bedding material seems to be an important comfort issue for claw health in dairy cows. The prevalence of claw lesions was less common in compost-bedded packs barns (CB)
than on free-stall (F) housed herds for heel horn erosion (26.9% CB and 59.5% in F), white line disease (20.4% CB and 46.6% in F) and interdigital hyperplasia (0.2% in C and 3.1% in F) (BURGSTALLER et al., 2016). The authors of that study argue that lower lesions might be observed in compost barn herds as a result of softer, dried ground and subsequent higher cleanliness of hooves on that system. The lameness prevalence, however, was the same on both housing systems.
The relationship between body size and facilities dimensions seems to influence cow comfort on resting, moving, standing or lying. Prolonged exposition to uneven or uncomfortable facilities might influence the posture of cows and, eventually, enhance the occurrence of lameness. Not fitting the average stall width increases the odds of being lame 3.7 and 1.3 times in primiparous and multiparous cows, respectively (WESTIN et al., 2016a). Cows on this conditions might be in constant uncomfortable conditions and may be unable of lying and rest appropriately.
Overstocking may be a factor influencing the stress on the cows’ foot. Increasing the available space for cows in holding yard has been associated with lower levels of lameness (RANJBAR et al., 2016). Inappropriate condition of structures or floors are also factors that might enhance the occurrence of lameness. Presence of damaged concrete on yards, or behaviors derived of inadequate fit of cows to facilities such as cows pushing each other or turning sharply near the parlor entrance, or exit, are associated with higher presentation of lameness (BARKER et al., 2010). The condition of paths or access areas to facilities might negatively affect the occurrence of lameness. The probability of severe lameness increased with no (4 times) or partly prepared (3.8 times) cover compared to prepared cover (BUROW et al., 2014).
2.4 EFFECTS OF NUTRITIONAL MANAGEMENT, MILK YIELD, BODY CONDITION SCORE AND PHYSIOLOGICAL STATUS OF THE TRANSITION COW ON LAMENESS
Two main risk factors for lameness associated with nutrition management of dairy cows have been identified: high milk production in early lactation and low body condition score (BCS) (BICALHO; MACHADO; CAIXETA, 2009; ALAWNEH et al., 2014; RANDALL et al., 2015). Apparently those factors may be intercorrelated. Cows that became lame produced more milk than control cows from the start of the lactation up to week 15 of lactation (BICALHO; WARNICK;
GUARD, 2008). In addition, cows that became lame also had loss of BCS in the first 4 (RANDALL et al., 2015) or between the 4-10 (HOEDEMAKER; PRANGE; GUNDELACH, 2009) weeks of lactation. Low BCS (<2, 3 weeks before) precedes repeated, or first lifetime (8-16 weeks after first parturition) lameness event in dairy cows (RANDALL et al., 2015). The association between BCS and lameness is present in different moments of lactation: cows with low BCS (2.75) at drying-off have greater occurrence of lameness (FODITSCH et al., 2016) and cows with BCS < 3 had greater occurrence of claw horn disruption lesions (CHDL), such as white line disease and sole ulcer (MACHADO et al., 2010).
Overall, the reduction in BCS is an indicator of body weight loss. In general, this association have two directions. Lame cows also lose weight (NORRING et al., 2014), due to the reduction in dry matter consumption, thus, body weight loss is, at the same time, an event that precedes the occurrence of new and chronic lameness cases, as well as a consequence of chronic cases of lameness. That fact constitutes a challenge for establishing causal relationships in cross-sectional studies. Loss of BCS increases the probability of lameness and decreases the likelihood of recovery over the next 15 days after the event (LIM et al., 2015), thus is not just the status of the BCS in a specific time, but also the dynamics of change of BCS (reflecting a measure of body weight loss and energy mobilization) (ALAWNEH et al., 2014) that contributes with the occurrence and persistence of lameness. That dynamics is also bidirectional: gain in BCS seems to be a protective factor for lameness (LIM et al., 2015).
The susceptibility of cows to loss BCS may be influenced by genetic selection, thus, cows predisposed to maintain good levels of body condition score seems to be less susceptible to have locomotion and lameness problems (KOUGIOUMTZIS et al., 2014). Selection for higher milk yield and protein production has been associated with specific claw lesions such as white line disease, sole ulcer and digital dermatitis (OIKONOMOU; COOK; BICALHO, 2013). This opens the possibility of thinking in genetic selection focused in hoof health in dairy cows as an interesting strategy to reduce lameness in dairy herds. Keeping an optimal BCS at critical periods of lactation curve, like dry off and transition period, seems to be important protective factors for non-infectious lameness.
Lactating cows experience radical metabolic changes throughout their productive life, specially on critical periods like the transition.
Those metabolic changes seems to have an important role on the physiopathology of non-infectious lameness. There is a positive association of BCS and digital cushion thickness (DCT) because a cow that is losing body weight mobilizes fat from all tissues, including the digital cushion (GREEN et al., 2014). The diminution of the digital cushion thickness might reduce the mechanisms of hoof damping and facilitate the traumatic lesions of the foot (RÄBER et al., 2004, 2006). Although there is not a specific causal demonstration of the relationship between DCT and lameness, their association seems to be strong (BICALHO; MACHADO; CAIXETA, 2009). Also, it seems to exists temporary association between the two events. Cows are more likely to become lame between 91-120 days in lactation an this coincides with the period where DCT is lower (LIM et al., 2015).
This way, like happens with another health issues in dairy cattle, cows seems to be more susceptible to non infectious lameness in the period around the parturition. Assuming a standard lactation curve, cows are more susceptible to reduce BCS on the first weeks of lactation. Cows with higher milk yield (on peak of lactation or high producer cows) demand more energy and mobilizes more fat from body reserves than other animals in order to supply mammary gland production. The risk of being lame was 4.4 times greater in high yielding grazing cows that lost live weight on first 50 days in milk, than in cows with lower yield. Thus, it has been proposed that high milk production on first weeks of lactation is a risk factor for lameness (OIKONOMOU; COOK; BICALHO, 2013; GREEN et al., 2014).
The association between milk yield and lameness is also bidirectional and dynamic (time-dependent): cows with greater milk yield are prone to became lame, and after became lame, milk yield is reduced, but the daily production increases again after the cow is treated early (LEACH et al., 2012). Because the BCS loss and higher milk yield are both indicators that reflect the metabolic status of the cow, lameness events seems to result as a consequence of the interaction between those and other risk factors such as parity, age, days in milk, genetic selection, comfort issues like individual daily lying time or inadequate lying behavior.
Given that multiple diseases or lesions may cause lameness, is important to know the risk factors for specific diseases or hoof lesions causing lameness (LAWRENCE; CHESTERTON; LAVEN, 2011). The risk factors for single lesions are more specific than the broad spectrum of lameness risk factors and thus are easier to identify (DIPPEL et al.,
2009). Studies assessing those specific risk factors for diseases causing lameness are scarce, but it seems that the relationship between milk production, BCS and digital cushion thinness is specifically associated with hoof horn dysfunction (i.e., CHDL) (MACHADO et al., 2010). Low BCS (< 2.5) is a risk factor for the principal non-infectious claw diseases: sole ulcer, white line disease and sole hemorrhages (GREEN et al., 2014).
Most lame cows are affected by hoof lesions located in the lateral claw of hind feet (Color Atlas of Diseases and Disorders of Cattle, 2011; HUXLEY et al., 2012). Thus, lameness associated with claw horn dysfunction seems to have a strong relationship with postural and mechanical forces acting on the skeleton and soft tissues of the cows. An important issue for understanding this dynamics is the asymmetry artiodactyls’ toe. Lateral toes are longer than medial toes in hooves of wild (KELLER et al., 2009) and domestic even-toed ungulates (MUGGLI et al., 2011). This might be a possible adaptation that helps to stabilize the body of the animal on soft floors, like natural habitats of bovines (MUGGLI et al., 2011). However, when bovines stand for a long time in hard floors, this anatomical configuration may lead to compression and reduced perfusion of the corium and may increase the occurrence of claw horn diseases such as sole ulcer (MUGGLI et al., 2011) as well as hypertrophy and deformation of the outer hoof (KELLER et al., 2009). Thus, dairy cows with access to comfortable floor surfaces to stand and with provision of suitable areas and conditions to lying in a proper manner should be at least risk of having claw disorders and lameness.
2.5 GRAZING, OUTDOOR ACCESS AND LAMENESS
Let the cows having access to pasture or to outdoor loafing areas in confined herds might be a protective factor for lameness (DIPPEL et al., 2009; ADAMS et al., 2017). Dairy cows housed in free-stall had improvement in gait score when had access to pasture for four weeks (HERNANDEZ-MENDO et al., 2007). Also, in a cross-sectional study was noticed that cows with access to pasture had less severe lameness prevalence than animals housed in free-stall or open dry lots (ADAMS et al., 2017). Additionally, the lameness occurrence seems to be lower in some studies conducted in populations of grazing dairy cows, if compared with the observed prevalence in some confined systems. A study on dairy cows (one farm) in New Zealand reported a lameness
incidence of 13% (ALAWNEH et al., 2014). The average lameness prevalence in grazing dairy herds in Australia was 19% (RANJBAR et al., 2016). However, lower lameness prevalence has been also reported recently in confined dairies in North America: 15% (WESTIN et al., 2016b) 14% (FODITSCH et al., 2016) 9.6% (ADAMS et al., 2017). Moreover, the variation in lameness occurrence between farms is high in the same study and studies in grazing systems are less common than studies conducted in confined systems which may be a source of bias for judging the relationship between lameness and housing.
The presence of many biological interactions and the multiple factors that contribute to the occurrence of lameness difficult to make inferences on housing systems (VON KEYSERLINGK; WEARY, 2017); thus, in order to make this comparison valid, it is important to consider potential confounders or intervening variables such as herd size, management, specific aspects of facility design and the use of effective preventive practices for lameness. Inferring from studies when comparisons are done at the population level, without considering the individual factors that contribute to the occurrence of lameness, may also be difficult, in large part, because there are multiple sources of bias mediating the associations at different levels of analyses (e.g., “ecological fallacy”). In addition, if the structure (e.g., parity, days in lactation of cows), spatial distribution (e.g., the hierarchical and heterogeneous division of population in herds and pens), and size of the study population is not considered, additional biases may exist further limiting the validity of the analyses; minimizing the value of the results to inform the public on practical implications of the study.
Thus, a direct comparison between confined and pasture housing, might not be fair, appropriate, or useful in terms of animal welfare and health improvement. On the other side, dairy grazing systems are not standardized as can be other housing systems and strong differences on weather, seasonal variation of feed supply, feeding practices and management, breeds, herd size and other factors might be present under the same classification of grazing housing system.
Possible protective effects of grazing for diseases causing lameness, might be mediated by the reduction on risk for specific conditions (i.e., sole ulcer), but, in turn, some factors that are common in grazing systems may potentially increase the probability of lameness occurrence. In fact, claw lesions such as white line disease, sole injury and axial disease, seems to be proportionally more frequent in grazing cows (LAWRENCE; CHESTERTON; LAVEN, 2011) while hoof
abnormalities such as sole damage (i.e., sole ulcer, double sole) has been found commonly in housed systems, if compared with grazing systems (NAVARRO; GREEN; TADICH, 2013). Access to pasture in cows housed in tie stall was associated with higher presence of digital dermatitis, white line separation and interdigital fibroma (CRAMER et al., 2009). Thus, the condition of paths, heat stress, or other comfort-related issues could be trigger factors increasing the lameness occurrence by enhancing risk factors for diseases like white line disease, foot root or digital dermatitis in grazing dairy cows.
Lying comfort has been mentioned as a protective factor for lameness in grazing cows. When compared with confined systems, higher (OLMOS et al., 2009a) but also lower (HERNANDEZ-MENDO et al., 2007) lying times have been reported in grazing cows under experimental conditions, but information about lying behavior in cows at pasture is limited. A study assessing lying time in grazing and confined herds showed that cows on both housing systems had equal lying times (NAVARRO; GREEN; TADICH, 2013). A mean daily lying time of 11 h (VON KEYSERLINGK et al., 2012), 10.6 h (SOLANO et al., 2016) and 11.4 h (WESTIN et al., 2016a) have been reported in dairy cows housed in confined systems. The mean daily lying times reported for grazing cows were 7.5 h (for primiparous cows), 8.5 h (for multiparous cows) (SEPÚLVEDA-VARAS; WEARY; VON KEYSERLINGK, 2014) and 15.2 h (NAVARRO; GREEN; TADICH, 2013). Thus, data on grazing dairy cows seems to be more variable, but studies are still limited regarding number of herds, cows and time repetitions. Knowing and appropriately measuring the average normal lying behavior of grazing dairy cows may be important indicator of cows’ welfare and health.
Cows of the same herd that were managed on pasture had less severe hoof lesions, better locomotion and reduced occurrence of lameness compared to confined cows (OLMOS et al., 2009b), however, the evidence on this issue is not completely conclusive, due to lack of more studies on the issue. In other similar study the access to pasture did not reduce the presence of sole hemorrhages, sole ulcers or heel-horn erosion, but seemed to be associated with a reduction of digital dermatitis (HAUFE et al., 2012). On this regard, analysis of the long term effects of access to pasture on limbs, joints, hooves and muscles development might be important, especially when the animals are exposed to grazing at early stages of life. Having access to an open space and exercise in calves affects the characteristics of the digital
cushion, hence, potentially increasing the shock absorbing capacity of this structure. Mean digital cushion volume and surface were higher (37% and 18% respectively), in calves with access to pasture and exercise area than in a control group (GARD et al., 2015). More conclusive studies on this issue should take into account the temporary dynamics of the foot development in grazing calves and heifers, as well as the specific causes of lameness on each situation and a feasible physiopathological paths to explaining the patterns in lameness causes in grazing systems.
3 COW- AND HERD-LEVEL FACTORS ASSOCIATED WITH LAMENESS IN SMALL-SCALE GRAZING DAIRY HERDS IN BRAZIL
3.1 INTRODUCTION
Lameness is a common issue that impairs the health and welfare of dairy cattle. Lameness negatively affects dairy herds by reducing the reproduction rate and milk yield. The cost of treatments and also the economic losses derived from involuntary culling affects seriously the dairy industry. The risk factors for lameness, or the relative importance of specific exposures, might differ for cows managed in grazing systems. For this reason, exploring lameness prevalence and incidence and risk factors in grazing herds may help to identify specific recommendations for the control and prevention of lameness in pasture-based systems. The aim of this study was to assess lameness occurrence in small-scale grazing dairy herds and to identify the associated cow-and herd-level risk factors.
3.2 MATERIALS AND METHODS
The present cross-sectional study was carried out in 2015, in the western part of Santa Catarina State in Brazil. It was part of a larger study with multiple objectives including the identification of risk factors for peripartum diseases (DAROS et al., 2017) and stakeholder views of lameness in grazing dairy herds (OLMOS et al., 2018). The study report was conducted in compliance with the STROBE Veterinary Statement for reporting observational studies in epidemiology (SARGEANT et al., 2016). All procedures outlined below were approved by the Ethics Committees on Research on Humans (Protocol # PP1237779) and Animals (Protocol # PP00949) of the Federal University of Santa Catarina, Brazil and the University of British Columbia Animal Care committee (Protocol # A15-0082).
The sample of herds was selected by convenience, with farmers recruited based on information provided by people working in the dairy sector in the region. To minimize selection bias, informants were only aware of the general objective of the study. Farms were selected based on the following criteria: a) herd size of at least 40 cows, b) farms with good accessibility from main urban centers in the region, c) cows housed on pasture for at least 16 h/d, c) use of dairy production,
